Abstract
Gene expression oscillators can structure biological events temporally and spatially. Different biological functions benefit from distinct oscillator properties. Thus, finite developmental processes rely on oscillators that start and stop at specific times, a poorly understood behavior. Here, we have characterized a massive gene expression oscillator comprising > 3,700 genes in Caenorhabditis elegans larvae. We report that oscillations initiate in embryos, arrest transiently after hatching and in response to perturbation, and cease in adults. Experimental observation of the transitions between oscillatory and non‐oscillatory states at high temporal resolution reveals an oscillator operating near a Saddle Node on Invariant Cycle (SNIC) bifurcation. These findings constrain the architecture and mathematical models that can represent this oscillator. They also reveal that oscillator arrests occur reproducibly in a specific phase. Since we find oscillations to be coupled to developmental processes, including molting, this characteristic of SNIC bifurcations endows the oscillator with the potential to halt larval development at defined intervals, and thereby execute a developmental checkpoint function.
Highlights
Gene expression oscillations occur in many biological systems as exemplified by circadian rhythms in metabolism and behavior (Panda et al, 2002), vertebrate somitogenesis (Oates et al, 2012), plant lateral root branching (Moreno-Risueno et al, 2010), and C. elegans larval development (Hendriks et al, 2014)
Previous reports agreed on the wide-spread occurrence of oscillatory gene expression in C. elegans larvae (Grün et al, 2014; Hendriks et al, 2014; Kim et al, 2013), the published data sets were either insufficiently temporally resolved or too short to characterize oscillations across C. elegans larval development
To understand the extent and features of these oscillations better, including their continuity throughout development, we performed two extended time course experiments to cover the entire period of post-embryonic development plus early adulthood at hourly resolution
Summary
Gene expression oscillations occur in many biological systems as exemplified by circadian rhythms in metabolism and behavior (Panda et al, 2002), vertebrate somitogenesis (Oates et al., 2012), plant lateral root branching (Moreno-Risueno et al, 2010), and C. elegans larval development (Hendriks et al, 2014). They are well-suited for timekeeping, acting as molecular clocks that can provide a temporal, and thereby spatial, structure for biological events (Uriu, 2016). It benefits from a phase-resetting mechanism to permit moderate realignments, if needed, to external time
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